Title: Evidence that contaminated surfaces contribute to the transmission of hospital pathogens and an overview of strategies to address contaminated surfaces in hospital settings
Abstract: Evidence that contaminated surfaces contribute to the transmission of hospital pathogens comes from studies modeling transmission routes, microbiologic studies, observational epidemiologic studies, intervention studies, and outbreak reports. This review presents evidence that contaminated surfaces contribute to transmission and discusses the various strategies currently available to address environmental contamination in hospitals. Evidence that contaminated surfaces contribute to the transmission of hospital pathogens comes from studies modeling transmission routes, microbiologic studies, observational epidemiologic studies, intervention studies, and outbreak reports. This review presents evidence that contaminated surfaces contribute to transmission and discusses the various strategies currently available to address environmental contamination in hospitals. Environmental surfaces were once thought to play a negligible role in the endemic transmission of nosocomial pathogens.1Rhame F.S. The inanimate environment.in: Bennett J.V. Brachmann P.S. Hospital infection. 4th ed. Lipincott-Raven, Philadelphia [PA]1998: 299-324Google Scholar However, recent data indicate that contaminated surfaces play an important role in the endemic and epidemic transmission of certain pathogens that cause health care-associated infections.2Otter J.A. Yezli S. French G.L. The role played by contaminated surfaces in the transmission of nosocomial pathogens.Infect Control Hosp Epidemiol. 2011; 32: 687-699Crossref PubMed Scopus (429) Google Scholar Clostridium difficile, methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci (VRE), norovirus, and multidrug-resistant (MDR) gram-negative rods including Acinetobacter baumannii share the ability to be shed from infected or colonized patients, survive on dry surfaces for extend periods, and are difficult to eradicate by cleaning and disinfection.2Otter J.A. Yezli S. French G.L. The role played by contaminated surfaces in the transmission of nosocomial pathogens.Infect Control Hosp Epidemiol. 2011; 32: 687-699Crossref PubMed Scopus (429) Google Scholar Whereas the role of contaminated surfaces in the transmission of some pathogens such as the spore-forming C difficile has been recognized for some time,3Samore M.H. Venkataraman L. DeGirolami P.C. Arbeit R.D. Karchmer A.W. Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea.Am J Med. 1996; 100: 32-40Abstract Full Text PDF PubMed Scopus (287) Google Scholar the importance of contaminated surfaces in the transmission of other pathogens such as MDR A baumannii has come to light only in recent years.4Nseir S. Blazejewski C. Lubret R. Wallet F. Courcol R. Durocher A. Risk of acquiring multidrug-resistant gram-negative bacilli from prior room occupants in the ICU.Clin Microbiol Infect. 2011; 17: 1201-1208Crossref PubMed Scopus (194) Google Scholar The continued emergence of antimicrobial resistance in gram-negative bacteria in particular means that effective prevention and control strategies are required urgently.5Peleg A.Y. Hooper D.C. Hospital-acquired infections due to gram-negative bacteria.N Engl J Med. 2010; 362: 1804-1813Crossref PubMed Scopus (998) Google Scholar The transmission routes of pathogens are complicated and difficult to investigate, so studies focused on the role of surfaces in transmission have been rare until relatively recently.2Otter J.A. Yezli S. French G.L. The role played by contaminated surfaces in the transmission of nosocomial pathogens.Infect Control Hosp Epidemiol. 2011; 32: 687-699Crossref PubMed Scopus (429) Google Scholar Data suggesting that contaminated surfaces play a role in transmission come from studies modeling transmission,6Lee B.Y. Wettstein Z.S. McGlone S.M. Bailey R.R. Umscheid C.A. Smith K.J. et al.Economic value of norovirus outbreak control measures in healthcare settings.Clin Microbiol Infect. 2010; 17: 640-646Crossref PubMed Scopus (27) Google Scholar, 7Lawley T.D. Clare S. Deakin L.J. Goulding D. Yen J.L. Raisen C. et al.Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens.Appl Environ Microbiol. 2010; 76: 6895-6900Crossref PubMed Scopus (92) Google Scholar, 8Oelberg D.G. Joyner S.E. Jiang X. Laborde D. Islam M.P. Pickering L.K. Detection of pathogen transmission in neonatal nurseries using DNA markers as surrogate indicators.Pediatrics. 2000; 105: 311-315Crossref PubMed Scopus (67) Google Scholar microbiologic studies in vitro and in situ,9Boyce J.M. Are the epidemiology and microbiology of methicillin-resistant Staphylococcus aureus changing?.JAMA. 1998; 279: 623-624Crossref PubMed Scopus (120) Google Scholar, 10Hayden M.K. Blom D.W. Lyle E.A. Moore C.G. Weinstein R.A. Risk of hand or glove contamination after contact with patients colonized with vancomycin-resistant enterococcus or the colonized patients’ environment.Infect Control Hosp Epidemiol. 2008; 29: 149-154Crossref PubMed Scopus (223) Google Scholar, 11Manian F.A. Griesenauer S. Senkel D. Setzer J.M. Doll S.A. Perry A.M. et al.Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.Infect Control Hosp Epidemiol. 2011; 32: 667-672Crossref PubMed Scopus (62) Google Scholar, 12Otter J.A. French G.L. Survival of nosocomial bacteria and spores on surfaces and inactivation by hydrogen peroxide vapor.J Clin Microbiol. 2009; 47: 205-207Crossref PubMed Scopus (142) Google Scholar observational epidemiologic studies,3Samore M.H. Venkataraman L. DeGirolami P.C. Arbeit R.D. Karchmer A.W. Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea.Am J Med. 1996; 100: 32-40Abstract Full Text PDF PubMed Scopus (287) Google Scholar, 4Nseir S. Blazejewski C. Lubret R. Wallet F. Courcol R. Durocher A. Risk of acquiring multidrug-resistant gram-negative bacilli from prior room occupants in the ICU.Clin Microbiol Infect. 2011; 17: 1201-1208Crossref PubMed Scopus (194) Google Scholar, 13Drees M. Snydman D. Schmid C. Barefoot L. Hansjosten K. Vue P. et al.Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci.Clin Infect Dis. 2008; 46: 678-685Crossref PubMed Scopus (208) Google Scholar, 14Shaughnessy M.K. Micielli R.L. DePestel D.D. Arndt J. Strachan C.L. Welch K.B. et al.Evaluation of hospital room assignment and acquisition of Clostridium difficile infection.Infect Control Hosp Epidemiol. 2011; 32: 201-206Crossref PubMed Scopus (231) Google Scholar, 15Huang S.S. Datta R. Platt R. Risk of acquiring antibiotic-resistant bacteria from prior room occupants.Arch Intern Med. 2006; 166: 1945-1951Crossref PubMed Scopus (392) Google Scholar, 16Hardy K.J. Oppenheim B.A. Gossain S. Gao F. Hawkey P.M. A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and patients’ acquisition of MRSA.Infect Control Hosp Epidemiol. 2006; 27: 127-132Crossref PubMed Scopus (198) Google Scholar intervention studies aimed at improving the efficacy of cleaning and disinfection,17Passaretti C.L. Otter J.A. Reich N.G. Myers J. Shepard J. Ross T. et al.An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms.Clin Infect Dis. 2013; 56: 27-35Crossref PubMed Scopus (155) Google Scholar, 18Boyce J.M. Havill N.L. Otter J.A. McDonald L.C. Adams N.M. Cooper T. et al.Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.Infect Control Hosp Epidemiol. 2008; 29: 723-729Crossref PubMed Scopus (196) Google Scholar, 19Hayden M.K. Bonten M.J. Blom D.W. Lyle E.A. van de Vijver D.A. Weinstein R.A. Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures.Clin Infect Dis. 2006; 42: 1552-1560Crossref PubMed Scopus (316) Google Scholar, 20Datta R. Platt R. Yokoe D.S. Huang S.S. Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants.Arch Intern Med. 2011; 171: 491-494Crossref PubMed Scopus (147) Google Scholar, 21Dancer S.J. White L.F. Lamb J. Girvan E.K. Robertson C. Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study.BMC Med. 2009; 7: 28Crossref PubMed Scopus (202) Google Scholar, 22Mayfield J.L. Leet T. Miller J. Mundy L.M. Environmental control to reduce transmission of Clostridium difficile.Clin Infect Dis. 2000; 31: 995-1000Crossref PubMed Scopus (234) Google Scholar and outbreak reports.23Denton M. Wilcox M.H. Parnell P. Green D. Keer V. Hawkey P.M. et al.Role of environmental cleaning in controlling an outbreak of Acinetobacter baumannii on a neurosurgical intensive care unit.J Hosp Infect. 2004; 56: 106-110Abstract Full Text Full Text PDF PubMed Scopus (161) Google Scholar, 24Zanetti G. Blanc D.S. Federli I. Raffoul W. Petignat C. Maravic P. et al.Importation of Acinetobacter baumannii into a burn unit: a recurrent outbreak of infection associated with widespread environmental contamination.Infect Control Hosp Epidemiol. 2007; 28: 723-725Crossref PubMed Scopus (68) Google Scholar, 25Thornley C.N. Emslie N.A. Sprott T.W. Greening G.E. Rapana J.P. Recurring norovirus transmission on an airplane.Clin Infect Dis. 2011; 53: 515-520Crossref PubMed Scopus (62) Google Scholar The role played by contaminated environmental surfaces in the transmission of nosocomial pathogens was recently reviewed.2Otter J.A. Yezli S. French G.L. The role played by contaminated surfaces in the transmission of nosocomial pathogens.Infect Control Hosp Epidemiol. 2011; 32: 687-699Crossref PubMed Scopus (429) Google Scholar Here, we present the latest data evaluating the role of contaminated surfaces in transmission and discuss the various strategies available to address environmental contamination in hospitals. Modeling transmission routes can provide “proof of principle” that contaminated surfaces are involved in transmission: for example, monitoring the spread of nonmicrobial markers,8Oelberg D.G. Joyner S.E. Jiang X. Laborde D. Islam M.P. Pickering L.K. Detection of pathogen transmission in neonatal nurseries using DNA markers as surrogate indicators.Pediatrics. 2000; 105: 311-315Crossref PubMed Scopus (67) Google Scholar the use of animal models,7Lawley T.D. Clare S. Deakin L.J. Goulding D. Yen J.L. Raisen C. et al.Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens.Appl Environ Microbiol. 2010; 76: 6895-6900Crossref PubMed Scopus (92) Google Scholar and mathematical modelling.6Lee B.Y. Wettstein Z.S. McGlone S.M. Bailey R.R. Umscheid C.A. Smith K.J. et al.Economic value of norovirus outbreak control measures in healthcare settings.Clin Microbiol Infect. 2010; 17: 640-646Crossref PubMed Scopus (27) Google Scholar One study evaluated the spread of a nonmicrobial marker (plant DNA) designed to model the spread of pathogens from hospitals surfaces. The marker was inoculated onto a single telephone handle in one of six 8-cot “pods” in a neonatal intensive care unit (ICU). The spread of the marker was remarkable: within 4 hours, it was identified from environmental surfaces and staff hands across the unit including all 6 pods. Whereas the spread of plant DNA does not necessarily accurately represent the spread of a pathogenic micro-organism, it does present a picture of dynamic and rapid transmission involving both environmental surfaces and staff hands. Another approach to modeling transmission is the use of animal models. For example, Lawley et al used a murine model to evaluate the transmission of C difficile.7Lawley T.D. Clare S. Deakin L.J. Goulding D. Yen J.L. Raisen C. et al.Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens.Appl Environ Microbiol. 2010; 76: 6895-6900Crossref PubMed Scopus (92) Google Scholar The model established that C difficile could be spread through experimentally contaminated cages in a dose-dependent manner. Furthermore, the model also demonstrated that disinfection of the cages using a range of disinfectants interrupted transmission proportionally to the level of spore reduction achieved. Mathematical modeling can also provide some insight into transmission routes. Mathematical models including the role of contaminated surfaces are rare, but one study evaluated the likely economic impact of various control strategies for norovirus including improved disinfection.6Lee B.Y. Wettstein Z.S. McGlone S.M. Bailey R.R. Umscheid C.A. Smith K.J. et al.Economic value of norovirus outbreak control measures in healthcare settings.Clin Microbiol Infect. 2010; 17: 640-646Crossref PubMed Scopus (27) Google Scholar The model found that increased disinfection alone or in combination with increased hand hygiene and using protective apparel were most useful for the control and containment of norovirus outbreaks. Environmental sampling of the surfaces surrounding patients in hospitals has established that certain pathogens are shed into the hospital environment. Wide variation in the reported frequency of environmental contamination can be explained by several factors, including the culturability of the organism, the degree of shedding by the patient, the sampling methodology, the ease of contamination (or difficulty of cleaning) of the particular environment, and whether there is an ongoing outbreak at the time of sampling. Surfaces in the vicinity of patients have a higher frequency of contamination than other sites.10Hayden M.K. Blom D.W. Lyle E.A. Moore C.G. Weinstein R.A. Risk of hand or glove contamination after contact with patients colonized with vancomycin-resistant enterococcus or the colonized patients’ environment.Infect Control Hosp Epidemiol. 2008; 29: 149-154Crossref PubMed Scopus (223) Google Scholar, 26Huslage K. Rutala W.A. Sickbert-Bennett E. Weber D.J. A quantitative approach to defining “high-touch” surfaces in hospitals.Infect Control Hosp Epidemiol. 2010; 31: 850-853Crossref PubMed Scopus (156) Google Scholar Infected patients shed more pathogens than those who are only colonized, and diarrhea results in widespread contamination.27Boyce J.M. Potter-Bynoe G. Chenevert C. King T. Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications.Infect Control Hosp Epidemiol. 1997; 18: 622-627Crossref PubMed Google Scholar, 28Boyce J.M. Opal S.M. Chow J.W. Zervos M.J. Potter-Bynoe G. Sherman C.B. et al.Outbreak of multidrug-resistant Enterococcus faecium with transferable vanB class vancomycin resistance.J Clin Microbiol. 1994; 32: 1148-1153PubMed Google Scholar Although the presence of a pathogen on a surface does not necessarily represent a risk for transmission,1Rhame F.S. The inanimate environment.in: Bennett J.V. Brachmann P.S. Hospital infection. 4th ed. Lipincott-Raven, Philadelphia [PA]1998: 299-324Google Scholar studies have demonstrated that the infectious dose of some pathogens is low. For example, a small number of C difficile spores or norovirus particles are sufficient to initiate an infection.7Lawley T.D. Clare S. Deakin L.J. Goulding D. Yen J.L. Raisen C. et al.Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens.Appl Environ Microbiol. 2010; 76: 6895-6900Crossref PubMed Scopus (92) Google Scholar, 29Yezli S. Otter J.A. Minimum infective dose of the major human respiratory and enteric viruses transmitted through food and the environment.Food Environ Microbiol. 2011; 3: 1-30Google Scholar, 30Larson H.E. Borriello S.P. Quantitative study of antibiotic-induced susceptibility to Clostridium difficile enterocecitis in hamsters.Antimicrob Agents Chemother. 1990; 34: 1348-1353Crossref PubMed Scopus (57) Google Scholar Microbiologic studies have established that certain hospital pathogens can survive on dry hospital surfaces for extend periods (Table 1).31Kramer A. Schwebke I. Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.BMC Infect Dis. 2006; 6: 130Crossref PubMed Scopus (1548) Google Scholar The survival of hospital pathogens on dry hospital surfaces in vitro varies according to experimental conditions, but some strains of vegetative bacteria have the capacity to survive for months on dry hospital surfaces. VRE in particular seems to have remarkable survival properties, with a recent study showing that VRE can remain viable on dry surfaces for almost 4 years.32Wagenvoort J.H. De Brauwer E.I. Penders R.J. Willems R.J. Top J. Bonten M.J. Environmental survival of vancomycin-resistant Enterococcus faecium.J Hosp Infect. 2011; 77: 282-283Abstract Full Text Full Text PDF PubMed Scopus (41) Google Scholar The mechanisms underlying this surprising survival capacity of certain vegetative bacteria are unknown, but the recent discovery of biofilms on dry hospital surfaces may provide a mechanism through which vegetative bacteria could survive on dry surfaces for such extend periods without a nutrient source.33Vickery K. Deva A. Jacombs A. Allan J. Valente P. Gosbell I.B. Presence of biofilm containing viable multiresistant organisms despite terminal cleaning on clinical surfaces in an intensive care unit.J Hosp Infect. 2012; 80: 52-55Abstract Full Text Full Text PDF PubMed Scopus (122) Google Scholar, 34Yezli S. Otter J.A. Does the discovery of biofilms on dry hospital environmental surfaces change the way we think about hospital disinfection?.J Hosp Infect. 2012; 81: 293-294Abstract Full Text Full Text PDF PubMed Scopus (12) Google ScholarTable 1Survival of hospital pathogens on dry hospital surfacesNOTE. Adapted from Kramer et al.31Kramer A. Schwebke I. Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.BMC Infect Dis. 2006; 6: 130Crossref PubMed Scopus (1548) Google ScholarOrganismSurvival timeClostridium difficile (spores)>5 MonthsAcinetobacter spp3 Days to 11 months79Wagenvoort J.H. Joosten E.J. An outbreak Acinetobacter baumannii that mimics MRSA in its environmental longevity.J Hosp Infect. 2002; 52: 226-227Abstract Full Text PDF PubMed Scopus (35) Google ScholarEnterococcus spp including VRE5 Days to >46 months32Wagenvoort J.H. De Brauwer E.I. Penders R.J. Willems R.J. Top J. Bonten M.J. Environmental survival of vancomycin-resistant Enterococcus faecium.J Hosp Infect. 2011; 77: 282-283Abstract Full Text Full Text PDF PubMed Scopus (41) Google ScholarPseudomonas aeruginosa6 Hours to 16 monthsKlebsiella spp2 Hours to >30 monthsStaphylococcus aureus, including MRSA7 Days to >12 months80Wagenvoort J.H. Sluijsmans W. Penders R.J. Better environmental survival of outbreak vs. sporadic MRSA isolates.J Hosp Infect. 2000; 45: 231-234Abstract Full Text PDF PubMed Scopus (149) Google ScholarNorovirus (and feline calicivirus)8 Hours to >2 weeks81Doultree J.C. Druce J.D. Birch C.J. Bowden D.S. Marshall J.A. Inactivation of feline calicivirus, a Norwalk virus surrogate.J Hosp Infect. 1999; 41: 51-57Abstract Full Text PDF PubMed Scopus (257) Google Scholar Open table in a new tab In vitro studies of the spread of DNA or other markers, model organisms, or pathogens show that transfer can occur from environmental surfaces to hands and vice versa.35Winther B. McCue K. Ashe K. Rubino J. Hendley J.O. Rhinovirus contamination of surfaces in homes of adults with natural colds: transfer of virus to fingertips during normal daily activities.J Med Virol. 2011; 83: 906-909Crossref PubMed Scopus (21) Google Scholar, 36Rusin P. Maxwell S. Gerba C. Comparative surface-to-hand and fingertip-to-mouth transfer efficiency of gram-positive bacteria, gram-negative bacteria, and phage.J Appl Microbiol. 2002; 93: 585-592Crossref PubMed Scopus (274) Google Scholar, 37Barker J. Vipond I.B. Bloomfield S.F. Effects of cleaning and disinfection in reducing the spread of Norovirus contamination via environmental surfaces.J Hosp Infect. 2004; 58: 42-49Abstract Full Text Full Text PDF PubMed Scopus (303) Google Scholar, 38Rheinbaben F. Schunemann S. Gross T. Wolff M.H. Transmission of viruses via contact in a household setting: experiments using bacteriophage straight phiX174 as a model virus.J Hosp Infect. 2000; 46: 61-66Abstract Full Text PDF PubMed Scopus (110) Google Scholar Several microbiologic studies have investigated the transfer of pathogens from surfaces to the hands or gloves of health care personnel in the absence of direct patient contact (Table 2). Contact with an environmental surface carries approximately the same risk of acquiring MRSA,39Stiefel U. Cadnum J.L. Eckstein B.C. Guerrero D.M. Tima M.A. Donskey C.J. Contamination of hands with methicillin-resistant Staphylococcus aureus after contact with environmental surfaces and after contact with the skin of colonized patients.Infect Control Hosp Epidemiol. 2011; 32: 185-187Crossref PubMed Scopus (122) Google Scholar VRE,10Hayden M.K. Blom D.W. Lyle E.A. Moore C.G. Weinstein R.A. Risk of hand or glove contamination after contact with patients colonized with vancomycin-resistant enterococcus or the colonized patients’ environment.Infect Control Hosp Epidemiol. 2008; 29: 149-154Crossref PubMed Scopus (223) Google Scholar and C difficile40Guerrero D.M. Nerandzic M.M. Jury L.A. Jinno S. Chang S. Donskey C.J. Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms.Am J Infect Control. 2012; 40: 556-558Abstract Full Text Full Text PDF PubMed Scopus (77) Google Scholar hand or glove contamination as touching an infected or colonized patient. One study estimated that VRE hand contamination was acquired through approximately 10% of contacts with either the patient or the surfaces surrounding the patient.10Hayden M.K. Blom D.W. Lyle E.A. Moore C.G. Weinstein R.A. Risk of hand or glove contamination after contact with patients colonized with vancomycin-resistant enterococcus or the colonized patients’ environment.Infect Control Hosp Epidemiol. 2008; 29: 149-154Crossref PubMed Scopus (223) Google Scholar Importantly, hand hygiene compliance was significantly more likely following direct patient contact compared with contact with the patient environment, meaning that contamination acquired from the environment is likely to persist for longer and hence could be relatively more important for onward transmission.41Randle J. Arthur A. Vaughan N. Twenty-four-hour observational study of hospital hand hygiene compliance.J Hosp Infect. 2010; 76: 252-255Abstract Full Text Full Text PDF PubMed Scopus (101) Google ScholarTable 2Transfer of pathogens from surfaces to the hands of health care personnelDirect patient contactContact with environmental surfaces only52% of 44 HCP acquired VRE on their hands or gloves10Hayden M.K. Blom D.W. Lyle E.A. Moore C.G. Weinstein R.A. Risk of hand or glove contamination after contact with patients colonized with vancomycin-resistant enterococcus or the colonized patients’ environment.Infect Control Hosp Epidemiol. 2008; 29: 149-154Crossref PubMed Scopus (223) Google Scholar45% of 50 HCP acquired MRSA on their gloved hands39Stiefel U. Cadnum J.L. Eckstein B.C. Guerrero D.M. Tima M.A. Donskey C.J. Contamination of hands with methicillin-resistant Staphylococcus aureus after contact with environmental surfaces and after contact with the skin of colonized patients.Infect Control Hosp Epidemiol. 2011; 32: 185-187Crossref PubMed Scopus (122) Google Scholar40% of 50 HCP acquired MRSA on their gloved hands39Stiefel U. Cadnum J.L. Eckstein B.C. Guerrero D.M. Tima M.A. Donskey C.J. Contamination of hands with methicillin-resistant Staphylococcus aureus after contact with environmental surfaces and after contact with the skin of colonized patients.Infect Control Hosp Epidemiol. 2011; 32: 185-187Crossref PubMed Scopus (122) Google Scholar50% of 30 HCP acquired Clostridium difficile on their gloved hands40Guerrero D.M. Nerandzic M.M. Jury L.A. Jinno S. Chang S. Donskey C.J. Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms.Am J Infect Control. 2012; 40: 556-558Abstract Full Text Full Text PDF PubMed Scopus (77) Google Scholar50% of 30 HCP acquired C difficile on their gloved hands40Guerrero D.M. Nerandzic M.M. Jury L.A. Jinno S. Chang S. Donskey C.J. Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms.Am J Infect Control. 2012; 40: 556-558Abstract Full Text Full Text PDF PubMed Scopus (77) Google ScholarCompliance with hand hygiene: 80%41Randle J. Arthur A. Vaughan N. Twenty-four-hour observational study of hospital hand hygiene compliance.J Hosp Infect. 2010; 76: 252-255Abstract Full Text Full Text PDF PubMed Scopus (101) Google ScholarCompliance with hand hygiene: 50%41Randle J. Arthur A. Vaughan N. Twenty-four-hour observational study of hospital hand hygiene compliance.J Hosp Infect. 2010; 76: 252-255Abstract Full Text Full Text PDF PubMed Scopus (101) Google ScholarHCP, Health care personnel. Open table in a new tab HCP, Health care personnel. Cleaning and/or disinfection is usually performed daily (or several times daily) to reduce the environmental burden and ensure that the patient environment remains visibly clean. More stringent cleaning and/or disinfection is performed at patient discharge (sometimes called “terminal” cleaning/disinfection) to ensure that the clinical area is properly disinfected and safe for the next occupant. Many studies have been performed to investigate the efficacy of cleaning and disinfection, and most focus on the efficacy of terminal cleaning/disinfection. Environmental sampling performed after terminal disinfection often identifies surfaces contaminated with the pathogen that the process is aiming to eliminate.18Boyce J.M. Havill N.L. Otter J.A. McDonald L.C. Adams N.M. 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Lack of enhanced effect of a chlorine dioxide-based cleaning regimen on environmental contamination with Clostridium difficile spores.J Hosp Infect. 2012; 82: 64-67Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar Even multiple “rounds” of bleach disinfection may not be sufficient to eliminate some pathogens.11Manian F.A. Griesenauer S. Senkel D. Setzer J.M. Doll S.A. Perry A.M. et al.Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.Infect Control Hosp Epidemiol. 2011; 32: 667-672Crossref PubMed Scopus (62) Google Scholar, 42Byers K.E. Durbin L.J. Simonton B.M. Anglim A.M. Adal K.A. Farr B.M. Disinfection of hospital rooms contaminated with vancomycin-resistant Enterococcus faecium.Infect Control Hosp Epidemiol. 1998; 19: 261-264Crossref PubMed Google Scholar, 46Morter S. Bennet G. Fish J. Richards J. Allen D.J. Nawaz S. et al.Norovirus in the hospital setting: virus introduction and spread within the hospital environment.J Hosp Infect. 2011; 77: 106-112Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar For example, a recent study found that 27% of rooms remained contaminated with A baumannii or MRSA following 4 rounds of bleach disinfection.11Manian F.A. Griesenauer S. Senkel D. Setzer J.M. Doll S.A. Perry A.M. et al.Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.Infect Control Hosp Epidemiol. 2011; 32: 667-672Crossref PubMed Scopus (62) Google Scholar Similarly, 43% of surfaces were contaminated with norovirus RNA after 1 round of bleach disinfection, and 16% of surfaces were c